Yeast axial-element protein, Red1, binds SUMO chains to promote meiotic interhomologue recombination and chromosome synapsis

EMBO J. 2010 Feb 3;29(3):586-96. doi: 10.1038/emboj.2009.362. Epub 2009 Dec 3.

Abstract

The synaptonemal complex (SC) is a tripartite protein structure consisting of two parallel axial elements (AEs) and a central region. During meiosis, the SC connects paired homologous chromosomes, promoting interhomologue (IH) recombination. Here, we report that, like the CE component Zip1, Saccharomyces cerevisiae axial-element structural protein, Red1, can bind small ubiquitin-like modifier (SUMO) polymeric chains. The Red1-SUMO chain interaction is dispensable for the initiation of meiotic DNA recombination, but it is essential for Tel1- and Mec1-dependent Hop1 phosphorylation, which ensures IH recombination by preventing the inter-sister chromatid DNA repair pathway. Our results also indicate that Red1 and Zip1 may directly sandwich the SUMO chains to mediate SC assembly. We suggest that Red1 and SUMO chains function together to couple homologous recombination and Mec1-Tel1 kinase activation with chromosome synapsis during yeast meiosis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Chromosome Pairing / physiology*
  • Crossing Over, Genetic
  • DNA-Binding Proteins / metabolism
  • Meiosis* / physiology
  • Nuclear Proteins / metabolism
  • Organisms, Genetically Modified
  • Phosphorylation
  • Protein Binding
  • Protein Interaction Domains and Motifs / physiology
  • Protein Multimerization / physiology
  • Recombination, Genetic / physiology*
  • SUMO-1 Protein / chemistry
  • SUMO-1 Protein / metabolism*
  • Saccharomyces cerevisiae / genetics
  • Saccharomyces cerevisiae / physiology
  • Saccharomyces cerevisiae Proteins / chemistry
  • Saccharomyces cerevisiae Proteins / metabolism*
  • Saccharomyces cerevisiae Proteins / physiology
  • Sequence Homology
  • Small Ubiquitin-Related Modifier Proteins / chemistry
  • Small Ubiquitin-Related Modifier Proteins / metabolism
  • Synaptonemal Complex / metabolism
  • Synaptonemal Complex / physiology

Substances

  • DNA-Binding Proteins
  • HOP1 protein, S cerevisiae
  • Nuclear Proteins
  • RED1 protein, S cerevisiae
  • SMT3 protein, S cerevisiae
  • SUMO-1 Protein
  • Saccharomyces cerevisiae Proteins
  • Small Ubiquitin-Related Modifier Proteins
  • Zip1 protein, S cerevisiae